Abstract
Plants express many calmodulin (CaM) isoforms. These proteins regulate the growth, development and environmental stress responses of plants by modulating targets. Herein, the Arabidopsis CaM2 isoform was found to be crucial for cold adaptation in prokaryotic cells, similar to the Escherichia coli cold shock protein CspA. Expressing CaM2 or CspA in the cold-sensitive E. coli BX04 mutant complemented the cold-sensitive phenotype under cold stress, but expression of CaM1, CaM7 or CML8 (CaM8) did not. Similar to RNA chaperones such as CspA, CaM2 strongly interacted with nucleic acids and its nucleic acid-binding capacity was much higher than that of CaM7, despite there being only a single amino acid difference between these two isoforms. Microscopic observation of CaM2-GFP revealed that CaM2 plays roles in both the nucleus and cytosol where RNA molecules are abundant. These results suggest that CaM2 can positively modulate cold stress responses by interacting with nucleic acid targets. Furthermore, CaM2 has both nucleic acid targets, similar to CaM7, and protein targets such as CAMTA3.
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Xin, Z. and J. Browse (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ. 23: 893–902.
Nedwell, D. B. (1999) Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol. Ecol. 30: 101–111.
DeFalco, T. A., K. W. Bender, and W. A. Snedden (2009) Breaking the code: Ca2+ sensors in plant signalling. Biochem. J. 425: 27–40.
Fernandes, I. P. and A. M. Oliveira–Brett (2017) Calciuminduced calmodulin conformational change. Electrochemical evaluation. Bioelectrochemistr. 113: 69–78.
Elizabeth, M. and B. Janet (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytologis. 159: 585–598.
Virdi, A. S., S. Singh, and P. Singh (2015) Abiotic stress responses in plants: roles of calmodulin–regulated proteins. Front Plant Sci. 6: 809.
Munir, S., H. Liu, Y. Xing, S. Hussain, B. Ouyang, Y. Zhang, H. Li, and Z. Ye (2016) Overexpression of calmodulin–like (ShCML44) stress–responsive gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses. Sci. Rep. 6: 31772.
Yang, N., C. Peng, D. Cheng, Q. Huang, G. Xu, F. Gao, and L. Chen (2013) The over–expression of calmodulin from Antarctic notothenioid fish increases cold tolerance in tobacco. Gen. 521: 32–37.
Doherty, C. J., H. A. Van Buskirk, S. J. Myers, and M. F. Thomashow (2009) Roles for Arabidopsis CAMTA transcription factors in cold–regulated gene expression and freezing tolerance. Plant Cel. 21: 972–984.
Chinnusamy, V., J. Zhu, and J. K. Zhu (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci. 12: 444–451.
Klinkert, B. and F. Narberhaus (2009) Microbial thermosensors. Cell Mol. Life Sci. 66: 2661–2676.
Narberhaus, F., T. Waldminghaus, and S. Chowdhury (2006) RNA thermometers. FEMS Microbiol. Rev. 30: 3–16.
Goldstein, J., N. S. Pollitt, and M. Inouye (1990) Major cold shock protein of Escherichia coli. Proc. Natl. Acad. Sci. US. 87: 283–287.
Jiang, W., Y. Hou, and M. Inouye (1997) CspA, the major coldshock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272: 196–202.
Kim, M. H. and R. Imai (2015) Determination of RNA chaperone activity using an Escherichia coli mutant. Methods Mol. Biol. 1259: 117–123.
Fischer, R., M. Koller, M. Flura, S. Mathews, M. A. Strehler–Page, J. Krebs, J. T. Penniston, E. Carafoli, and E. E. Strehler (1988) Multiple divergent mRNAs code for a single human calmodulin. J. Biol. Chem. 263: 17055–17062.
Bender, K. W. and W. A. Snedden (2013) Calmodulin–related proteins step out from the shadow of their namesake. Plant Physiol. 163: 486–495.
Abbas, N., J. P. Maurya, D. Senapati, S. N. Gangappa, and S. Chattopadhyay (2014) Arabidopsis CAM7 and HY5 physically interact and directly bind to the HY5 promoter to regulate its expression and thereby promote photomorphogenesis. Plant Cel. 26: 1036–1052.
Masui, Y., J. Coleman, and M. Inouye (1983) CHAPTER 2-multipurpose expression cloning vehicles in Escherichia coli, in experimental manipulation of gene expression. Academic Press 15–32.
Xia, B., H. Ke, and M. Inouye (2001) Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli. Mol. Microbiol. 40: 179–188.
Johnson, C. K. and G. S. Harms (2016) Tracking and localization of calmodulin in live cells. Biochim. Biophys. Act. 1863: 2017–2026.
Gong, Z., C.-H. Dong, H. Lee, J. Zhu, L. Xiong, D. Gong, B. Stevenson, and J.-K. Zhu (2005) A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cel. 17: 256–267.
Kim, J. S., S. J. Park, K. J. Kwak, Y. O. Kim, J. Y. Kim, J. Song, B. Jang, C. H. Jung, and H. Kang (2007) Cold shock domain proteins and glycine–rich RNA–binding proteins from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli. Nucleic Acids Res. 35: 506–516.
Kwak, K. J., Y. O. Kim, and H. Kang (2005) Characterization of transgenic Arabidopsis plants overexpressing GR–RBP4 under high salinity, dehydration, or cold stress. J. Exp. Bot. 56: 3007–3016.
Lee, S. H., J. D. Johnson, M. P. Walsh, J. E. Van Lierop, C. Sutherland, A. Xu, W. A. Snedden, D. Kosk–Kosicka, H. Fromm, N. Narayanan, and M. J. Cho (2000) Differential regulation of Ca2+/calmodulin–dependent enzymes by plant calmodulin isoforms and free Ca2+ concentration. Biochem. J. 350: 299–306.
Yoo, J. H., C. Y. Park, J. C. Kim, W. D. Heo, M. S. Cheong, H. C. Park, M. C. Kim, B. C. Moon, M. S. Choi, Y. H. Kang, J. H. Lee, H. S. Kim, S. M. Lee, H. W. Yoon, C. O. Lim, D.-J. Yun, S. Y. Lee, W. S. Chung, and M. J. Cho (2005) Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J. Biol. Chem. 280: 3697–3706.
Reddy, V. S., F. Safadi, R. E. Zielinski, and A. S. N. Reddy (1999) Interaction of a kinesin–like protein with calmodulin isoforms from Arabidopsis. J. Biol. Chem. 274: 31727–31733.
Yamniuk, A. P. and H. J. Vogel (2005) Structural investigation into the differential target enzyme regulation displayed by plant calmodulin isoforms. Biochemistr. 44: 3101–3111.
Kumar, S., M. Mazumder, N. Gupta, S. Chattopadhyay, and S. Gourinath (2016) Crystal structure of Arabidopsis thaliana calmodulin 7 and insight into its mode of DNA binding. FEBS Lett. 590: 3029–3039.
Perochon, A., D. Aldon, J.-P. Galaud, and B. Ranty (2011) Calmodulin and calmodulin–like proteins in plant calcium signaling. Biochimi. 93: 2048–2053.
Acknowledgments
This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (no. 2016R1D1A3B03930535) and by the Ministry of Science, ICT & Future Planning (no. 2015R1C1A2A01054562), Republic of Korea.
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Cheong, M.S., Chi, YH., Lee, JY. et al. Calmodulin 2 Functions as an RNA Chaperone in Prokaryotic Cells. Biotechnol Bioproc E 23, 448–455 (2018). https://doi.org/10.1007/s12257-018-0172-1
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DOI: https://doi.org/10.1007/s12257-018-0172-1